Equine Herpesvirus type 1 modulates cytokine and chemokine profiles of mononuclear cells for efficient dissemination to target organs.

Pavulraj, Selvaraj; Kamel, Mohamed; Stephanowitz, Heike; Liu, Fan; Plendl, Johanna; Osterrieder, Nikolaus; Azab, Walid

doi:10.3390/v12090999

Cited by 13Herpesvirus Infections and TreatmentsAnimal Virus Infections StudiesViral-associated cancers and disorders

Equine Herpesvirus type 1 modulates cytokine and chemokine profiles of mononuclear cells for efficient dissemination to target organs.

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Pavulraj, Selvaraj, Kamel, Mohamed, Stephanowitz, Heike, Liu, Fan, Plendl, Johanna, Osterrieder, Nikolaus, Azab, Walid·2020·Viruses

DOI 10.3390/v12090999PMC PMC7551999

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Abstract

Equine herpesvirus type 1 (EHV-1) causes encephalomyelopathy and abortion, for which cell-associated viremia and subsequent virus transfer to and replication in endothelial cells (EC) are responsible and prerequisites. Viral and cellular molecules responsible for efficient cell-to-cell spread of EHV-1 between peripheral blood mononuclear cells (PBMC) and EC remain unclear. We have generated EHV-1 mutants lacking ORF1, ORF2, and ORF17 genes, either individually or in combination. Mutant viruses were analyzed for their replication properties in cultured equine dermal cells, PBMC infection efficiency, virus-induced changes in the PBMC proteome, and cytokine and chemokine expression profiles. ORF1, ORF2, and ORF17 are not essential for virus replication, but ORF17 deletion resulted in a significant reduction in plaque size. Deletion of ORF2 and ORF17 gene significantly reduced cell-to-cell virus transfer from virus-infected PBMC to EC. EHV-1 infection of PBMC resulted in upregulation of several pathways such as Ras signaling, oxidative phosphorylation, platelet activation and leukocyte transendothelial migration. In contrast, chemokine signaling, RNA degradation and apoptotic pathways were downregulated. Deletion of ORF1, ORF2 and ORF17 modulated chemokine signaling and MAPK pathways in infected PBMC, which may explain the impairment of virus spread between PBMC and EC. The proteomic results were further confirmed by chemokine assays, which showed that virus infection dramatically reduced the cytokine/chemokine release in infected PBMC. This study uncovers cellular proteins and pathways influenced by EHV-1 after PBMC infection and provide an important resource for EHV-1 pathogenesis. EHV-1-immunomodulatory genes could be potential targets for the development of live attenuated vaccines or therapeutics against virus infection.

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Release of cytokines and chemokines is significantly reduced in PBMC upon EHV-1 infection.
“However, another study demonstrated that the release of cytokines and chemokines is significantly reduced in PBMC upon EHV-1 infection (Pavulraj et al., 2020).”
From The Pathogenesis and Immune Evasive Mechanisms of Equine Herpesvirus Type 1 (2021) · cites this paper as Pavulraj et al., 2020

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The Pathogenesis and Immune Evasive Mechanisms of Equine Herpesvirus Type 1
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Identification of Host Factors Associated with the Development of Equine Herpesvirus Myeloencephalopathy by Transcriptomic Analysis of Peripheral Blood Mononuclear Cells from Horses
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Double and quadruple deletion mutant of EHV-1 is highly attenuated and induces optimal immune response
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Recombinant Glycoprotein B of Equine herpesvirus Type 1 Elicits Protective Immune Response against Challenge in BALB/c Mouse Model
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Molecular characterization and pathogenesis of equine and elephant herpesviruses
Pavulraj, S. (2019) · doi:10.17169/refubium-26036
Equine herpesvirus type-1 modulates CCL2, CCL3, CCL5, CXCL9, and CXCL10 chemokine expression
Wimer, C. L., DAMIANI, A. M., Osterrieder, N., & Wagner, B. (2011) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2011.01.009 · Cited by 37 · see citing works
Transcriptomic Profiling of Equine and Viral Genes in Peripheral Blood Mononuclear Cells in Horses during Equine Herpesvirus 1 Infection
Zarski, L. M., Weber, P. S. D., Lee, Y., & Hussey, G. S. (2021) · Pathogens · doi:10.3390/pathogens10010043 · Cited by 12 · see citing works
The deletion of the ORF1 and ORF71 genes reduces virulence of the neuropathogenic EHV-1 strain Ab4 without compromising host immunity in horses
Wimer, C. L., Schnabel, C. L., Perkins, G. A., Babasyan, S., Freer, H., Stout, A. E., Rollins, A., Osterrieder, N., Goodman, L. B., Glaser, A. L., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0206679 · Cited by 33 · see citing works
Increased susceptibility of peripheral blood mononuclear cells to equine herpes virus type 1 infection upon mitogen stimulation: a role of the cell cycle and of cell-to-cell transmission of the virus
van der Meulen, K. M., Nauwynck, H., & Pensaert, M. B. (2002) · Veterinary Microbiology · doi:10.1016/s0378-1135(01)00499-0 · Cited by 11 · see citing works

Authors: Pavulraj, S., Kamel, M., Stephanowitz, H., Liu, F., Plendl, J., Osterrieder, N., & Azab, W.
Affiliations: Freie Universität Berlin (DE)
Cairo University (EG)
Leibniz-Forschungsinstitut für Molekulare Pharmakologie (DE)
Corresponding author: Azab, Walid
ORCID: Pavulraj, Selvaraj
Kamel, Mohamed
Liu, Fan
Plendl, Johanna
Osterrieder, Nikolaus
Azab, Walid
Venue: Viruses
Publisher: MDPI AG
Published: 2020-09-08
Volume: 12
Issue: 9
Pages: 999
ISSN: 1999-4915 (ISSN-L)
DOI: 10.3390/v12090999
PMC: PMC7551999
OpenAlex: W3084183380
Cited by: 13
References: 112
Citations by year: 2024: 2 · 2023: 3 · 2022: 3 · 2021: 5
FWCI: 1.97
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Viruses (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Refubium (Universitätsbibliothek der Freien Universität Berlin) (submittedVersion, cc-by)
Universitätsbibliothek der FU Berlin Hochschulschriftenstelle u. Dokumentenserver (cc-by)
Funders: Deutsche Forschungsgemeinschaft (DFG AZ 97/3-2)
Morris Animal Foundation (D19EQ-003)
U.S. Department of Agriculture (2018-67015-28242)
Topics: Health Sciences › Medicine › Epidemiology › Herpesvirus Infections and Treatments
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
Health Sciences › Medicine › Oncology › Viral-associated cancers and disorders
Keywords: equine herpesvirus 1, peripheral blood mononuclear cells, endothelial cells, ORF2, ORF1, viral mutants, proteome changes, Ras signaling, MAPK signaling, chemokine signaling, immunomodulation, encephalomyelopathy, abortion (veterinary)
MeSH terms: Animals, Herpesvirus 1, Equid, Herpesviridae Infections, Horse Diseases, Horses, Leukocytes, Mononuclear, Virus Replication, Cytokines, Chemokines, Host-Pathogen Interactions

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Equine Herpesvirus type 1 modulates cytokine and chemokine profiles of mononuclear cells for efficient dissemination to target organs.

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